A comparison in knee flexor and extensor strength following ACL reconstruction in international, male soccer players receiving patellar tendon or hamstrings grafts

The aim of this study was to compare knee extensor and flexor strength recovery following anterior cruciate ligament (ACL) reconstruction between bone-patellar tendon-bone (BPTB) and hamstring tendon (HT) grafts in international male soccer players undergoing comparable 6-month rehabilitation programmes. Seventeen players underwent ACL reconstruction with either an autogenous BPTB graft or HT graft. Knee extensor and flexor peak torques were measured at 3 months and 6 months in the injured and contralateral legs following surgery using isokinetic dynamometry. The moderate–large asymmetries in knee extensor peak torque between legs at 3 months across graft types (BPTB: p = 0.002, g = -0.94; HT: p = 0.02, g = -0.55) were reduced to trivial asymmetries at 6 months (BPTB: p = 0.30, g = -0.19; HT: p = 0.40, g = -0.16), with a non-significant difference in limb symmetry index (LSI) between grafts at 6 months (p = 0.62, g = -0.24). Similarly, moderate–large asymmetries in knee flexor peak torque between legs at 3 months across graft types (BPTB: p = 0.13, g = -0.50; HT: p = 0.01, g = -0.97) were reduced to trivial-small asymmetries at 6 months (BPTB: p = 0.25, g = 0.18; HT: p = 0.01, g = -0.47); however, a superior LSI was evident with BPTB compared to HT grafts at 6 months (p = 0.007, g = 1.43, large). Strength and conditioning professionals working with soccer players who are rehabilitating from ACL reconstruction after receiving a HT graft should give adequate attention to delivering suitable hamstring exercises that ensure optimal strength restoration.


INTRODUCTION
Soccer is the most popular team sport worldwide, with more than 275 million active players [1].Soccer players perform a range of intense movements, such as accelerations, decelerations, jumps, kicks, changes in direction, and tackles during training and matches.
In turn, many scenarios surrounding these movements including being tackled or tackling an opponent, regaining balance following kicking, and landing from jumping have been observed to take place when professional soccer players sustain an anterior cruciate ligament (ACL) injury [2].The incidence rate of ACL injury in European professional male soccer players has been reported to range from 0.04 to 0.06 per 1000 h of combined training and match exposure [3][4][5].In turn, ACL injuries are among the most devastating injuries encountered by professional soccer players, requiring extensive rehabilitation involving long lay-off times from training and competition [6].The return time to competition of professional soccer players is particularly important given the economic and performance A comparison in knee flexor and extensor strength following ACL reconstruction in international, male soccer players receiving patellar tendon or hamstrings grafts professional male soccer players for greater specificity in evidence for application in this population.

MATERIALS AND METHODS
This study adopted a within-(inter-limb comparisons) and betweensubject (BPTB vs. HT autografts) design to compare knee extensor and flexor strength recovery following ACL reconstruction in international male soccer players undergoing comparable 6-month rehabilitation programmes.Data were gathered at a private physiotherapy fitness centre Femur over a 4-year period until December 2022.
All procedures were approved by the Human Research Ethics Committee of the Faculty of Medical Sciences at University of Kragujevac, in Serbia (01-11122) in accordance with the Helsinki Declaration.
Subjects were able to participate in the study if free from any significant meniscus lesions (only a partial meniscectomy at most), chondral damage (as assessed either from magnetic resonance imaging or by the orthopaedic surgeon at the time of surgery), previous ACL injury (in the injured or contralateral leg), and other musculoskeletal injuries Although a slight predominance of one leg over the other is common in soccer players [14], inter-limb asymmetries in knee extensor and flexor strength of > 10% have been suggested to raise knee injury risk [15].In this regard, adequate functional recovery following ACL reconstruction is accepted when strength in the injured leg in relation to the contralateral leg reaches a limb symmetry index (LSI) of ≥ 90% [16].In contrast, inadequate knee extensor strength following ACL reconstruction yields greater rates and magnitudes of load transmission from distal to proximal segments of the leg to increase the risk of ACL graft re-rupture, contralateral knee injury, or premature degenerative changes in the repaired knee joint [2,17].Also, optimizing knee flexor strength is crucial when undergoing rehabilitation following ACL reconstruction given that this muscle group buffers shear forces by preventing anterior slide of the tibia relative to the femur [18].Furthermore, hamstring activation stabilizes the knee in response to external varus and valgus loads [19].Despite the importance of restoring knee extensor and flexor strength following ACL reconstruction, low rates of competitive [20] and professional [6] male soccer players with BPTB [6,20] and HT grafts [6] have been reported to achieve the desired LSI of ≥ 90% at 6-9 months following surgery [20] or when returning to unrestricted play [6].
Nevertheless, there is a lack of data directly comparing knee extensor and flexor strength recovery between BPTB and HT autografts in professional male soccer players.Such a comparison is essential given that graft type selection for ACL reconstruction may influence muscle strength recovery and therefore the duration required for a safe return to competition [21].
While there has been a lack of research on this topic specifically in soccer players, comparisons in strength recovery following ACL reconstruction between different graft types have been conducted in recreationally active individuals [22][23][24], non-athletes [25], non-professional athletes [26-29], military cadets [30], and athletes competing at varying playing levels pooled together [31,32].In addition to varied activity and playing levels, the available data have largely been pooled across athletes competing in different sports [27,28,30] and across sexes [21][22][23][24][25][26][27][28][30][31][32].Although these studies provide important insight into strength recovery following ACL reconstruction, the existing evidence may not be transferable to professional male soccer players considering that higher strength capacities have been observed in players competing at this playing level compared to lower levels [33].Furthermore, professional soccer players likely have greater access to wider resources (e.g., practitioner supervision, facilities, equipment) during the rehabilitation process compared to players competing at lower playing levels, aiding player recovery.Likewise, evidence stemming from pooled findings across players competing in different sports [27, 28, 30] and across sexes [21][22][23][24][25][26][27][28][30][31][32] should not be simply applied to male soccer players, given the different knee extensor and flexor strength levels reported according to these factors [34] and varied approaches adopted in managing the rehabilitation process [16].Therefore, examination of knee strength recovery following ACL reconstruction should be conducted strictly in Biology of Sport, Vol.41 No1, 2024 109 Effects of graft types on strength following ACL surgery that could negatively affect the results of the study.Accordingly, 4 of the 21 soccer players originally recruited were excluded, leaving 17 players (from Serbia, Croatia, Ukraine and Switzerland) participating in the study.All subjects provided written informed consent after the procedures of the study were explained, including the risks and benefits associated with participation.

Procedures
Subjects were allocated to the BPTB or HT group based on the autograft technique used for their ACL reconstruction.Both the BPTB and HT grafts were secured on the femur and tibia using interference screws.In the BPTB group, the central third of the patellar tendon was harvested with a vertical incision by blocking the patellar and tibial bones.A standard longitudinal incision over the pes anserinus was used for harvesting the HT graft.The BPTB autograft was between 9 and 10 mm in diameter, while the HT autograft was between 7 and 9 mm in diameter.All operations were performed by the same orthopaedic surgeon who specialized in conducting both ACL reconstruction techniques.The technique was selected for each subject according to their own choice with input from the surgeon.Injuries to both the dominant and non-dominant legs were involved in the sample (dominant leg: n = 7; non-dominant leg: n = 10).All subjects underwent the same standardized 6-month rehabilitation programme at the same private physiotherapy fitness centre.Isokinetic knee (extension and flexion) muscle strength was measured at 3 months and 6 months following surgery during the rehabilitation process.All testing sessions were carried out in similar environmental conditions for all subjects (~22 °C and ~60% relative humidity) and at a similar time of day (09:00 to 11:00).A verbal explanation and demonstration of the testing procedures were given to each subject prior to each testing session.Subjects completed a standardized warm-up prior to the isokinetic strength tests, consisting of a 5-min moderateintensity exercise bout on a cycle ergometer (Group Cycle Ride, Tech-noGym, Gambettola, Italy) [37, 38] followed by passive stretching exercises focused on the quadriceps, hamstrings, hip adductors, and calf muscles [39], as well as three submaximal knee extension and flexion movements for each leg at an angular speed of 60° • s −1 .
Stretching positions were held for short durations (15 s per muscle group) to avoid any subsequent negative impacts on performance [38] and ensure that proper body alignment was attained, involving subjects being in a comfortable and correct position that optimizes range of motion without causing pain [39,40].This study extends upon smaller scale exploratory research examining isokinetic knee extension and flexion strength recovery in 8 of the players examined without comparisons between graft types [41].

Rehabilitation
Subjects followed a 6-month rehabilitation programme, which involved a 90-min session delivered on 6 days per week under the supervision of the same physical therapist, who was highly experienced in managing soccer players following ACL reconstruction.
Rehabilitative progression was determined for each subject using criteria in published guidelines [17,42].The rehabilitation programme was divided into phases based on the stage of tissue recovery and the ability of the knee joint to withstand loading demands (0-4 weeks, 5-8 weeks, 9-12 weeks, 13-18 weeks, and 19-24 weeks).During the first 3 days following surgery, focus was placed on range of motion (gradual progress with ~90° achieved by the end of week 1 and full knee flexion achieved in week 4 or 5) as well as managing pain and swelling.Subjects were on crutches for 2 weeks following surgery, after which full weight bearing was permitted as tolerated.
Hydrotherapy was implemented for 2 weeks (e.g., deep water running, lunging, squatting, underwater cycling) 18 days after thread removal (thread removal was 16-18 days following surgery across subjects).Electrical stimulation (Compex SP 2.0; Compex Medical, Switzerland) was administered for 4 weeks after surgery to reduce the arthrogenic muscle inhibition effects of swelling, support the recovery of knee extensor strength, and activate the inhibited motoneurons.Movement complexity and speed of activities were systematically increased across isometric, isotonic, and isokinetic exercises.
The rehabilitation protocol followed by subjects has been previously described in detail [41].The load ratio for the quadriceps in seated knee extensions and hamstrings in seated leg curls differed between groups for the first 4 months of the rehabilitation programme (i.e., quadriceps:hamstrings of 60:40 for BPTB group and 40:60 for HT group).The quadriceps and hamstring muscles were equally loaded in both groups (i.e., 50:50) in months 5 and 6 of the rehabilitation programme.

Isokinetic muscle strength
Knee extensor and flexor peak torques were measured at 3 months and 6 months following surgery using an isokinetic dynamometer (HUMAC-NORM, Model 770; Computer Sports Medicine Inc., Stoughton, MA, USA).The reliability (intraclass correlation coefficient = 0.82-0.93,typical error = 5.7-7.7 N • m) of the isokinetic dynamometer at an angular velocity of 60° • s −1 has been supported previously [43].Each isokinetic strength test was performed in the concentric-concentric mode at an angular velocity of 60° • s −1 , which has been suggested to be the most sensitive in capturing asymmetries between legs in peak torque measurements for the knee extensors and flexors in athletes who have undergone ACL reconstruction [44].
Subjects were seated in a chair with hips flexed to 90°.The trunk was fixed to the chair with two straps crossing the chest and a further strap positioned across the waist.Handles on either side of the chair were grasped during testing for consistent arm positioning.Straps were fastened across the thigh and malleoli on the tested leg to restrict any lateral movement, allowing only flexion and extension at the knee.The contralateral leg was fixed with the foot positioned behind an ankle stabilizer.Subjects performed five extension and flexion movements interspersed with 2 min of passive rest between movement types.Standardized instructions and verbal encouragement were given to each subject during testing.The contralateral leg was assessed comparisons between timepoints, between legs, or between muscle groups were examined using paired t-tests.Post-hoc comparisons between graft groups were examined using unpaired t-tests.Hedge's g (with 95% confidence intervals [CI]) was also calculated to determine the ES for all post-hoc pairwise comparisons and was interpreted as [46]: trivial (< 0.20); small (0.20-0.49); moderate (0.50-0.79); or large (≥ 0.80).Statistical analyses were performed using IBM SPSS software (version 19; IBM Corp., Armonk, NY, USA).
Statistical significance was accepted at p < 0.05.

RESULTS
The results of each mixed ANOVA are presented in Table 1, with the mean ± SD for each outcome measure presented in Figure 1.Individual data, the median, minimum, maximum, and corresponding interquartile (25 th and 75 th percentiles) range in knee extensor peak torque, knee flexor peak torque, the H:Q for the injured and contralateral leg, as well as the LSI for the knee extensors and flexors at 3 months and 6 months following surgery are shown in Figure 2.
A 2 × 2 × 2 mixed ANOVA revealed a significant time*leg interaction (p < 0.001, η 2 = 0.64), with subsequent significant main effects of time (p < 0.001, η 2 = 0.67) and leg (p < 0.001, η 2 = 0.55) in knee extensor peak torque.Follow-up comparisons (Figure 3a) revealed a significant moderate increase in knee extensor peak torque in the injured leg between 3 months and 6 months across both graft types (BPTB: p < 0.001, g = 0.80; HT: p = 0.01, g = 0.54), whereas a significantly small increase (BPTB: p = 0.04, g = 0.21) and non-significant trivial increase (HT: p = 0.36, g = 0.17) were observed in the contralateral leg between these timepoints.In addition, significant moderate-large asymmetries in knee extensor peak torque between the injured and contralateral legs at 3 months for both graft types (BPTB: p = 0.002, g = -0.94;HT: p = 0.02, g = -0.55)were reduced to non-significant trivial first, followed by the injured leg using the same procedure with a 3-min passive resting period applied between legs.The highest peak torque (N • m) values recorded during knee extension and flexion were taken separately as outcome measures for each leg.LSI between legs and hamstrings:quadriceps ratio (H:Q) (concentric phase) within each leg were calculated as follows:

Statistical analysis
An a priori power analysis using G*power software (version 3.1.9.4; Heinrich Heine University Düsseldorf, Düsseldorf, Germany) recommended a sample size of 16 players using an estimated effect magnitude based on research examining isokinetic muscle strength at 3 months and 6 months following ACL reconstruction in a subset of the present sample (p = 0.05, effect size [ES] = 0.30; power = 0.80) [41].Normality of all data was confirmed using the Shapiro-Wilks test.Consequently, all data were reported as mean ± standard deviation (SD).Differences in outcome measures between BPTB graft and HT graft groups (graft effect), time points at 3 months and 6 months (time effect), injured and contralateral legs (leg effect), and muscle groups (muscle effect) were examined using separate 2 × 2 × 2 mixed analyses of variance (ANOVAs) with two withinsubjects factors (either time and leg effects or time and muscle effects), and one between-subjects factor (graft effect).Partial eta-squared (η 2 ) was utilized to indicate the ES for each mixed ANOVA, and was interpreted as [45]: no effect (≤ 0.04); minimum effect (0.05-0.25); moderate effect (0.26-0.64); or strong effect (> 0.65).Post-hoc TABLE 1. Statistical outcomes from the mixed ANOVAs showing time (3 months vs. 6 months), leg (injured vs. contralateral legs) or muscle (knee flexor limb symmetry index vs.knee extensor limb symmetry index), graft (bone-patellar tendon-bone vs. hamstrings tendon grafts), and interaction effects for knee extensor peak torque, knee flexor peak torque, peak torque hamstrings:quadriceps ratio (H:Q), and limb symmetry index in international, male soccer players who underwent anterior cruciate ligament reconstruction.differences between legs at 6 months (BPTB: p = 0.30, g = -0.19;
A 2 × 2 × 2 mixed ANOVA revealed non-significant interactions and main effects across all comparisons for H:Q, with non-significant trivial-moderate effects evident for all follow-up pairwise comparisons (Figure 4a).

FIG. 3.
Statistical pairwise comparisons for (a) knee extensor peak torque and (b) knee flexor peak torque between timepoints, legs, and graft types in international male soccer players.

DISCUSSION
The present results revealed that knee extensor peak torque was almost equivalent (BPTB: 0%; HT: 3%) to the contralateral leg regardless of the graft type used at 6 months following ACL reconstruction.Specifically, moderate-large asymmetries between legs in knee extensor peak torque at 3 months following reconstruction were reduced to trivial magnitudes at 6 months, with a desired difference of < 10% between legs across both graft types (BPTB: 6%; HT: 3%).Similarly, moderate-large asymmetries between legs in knee flexor peak torque at 3 months following reconstruction were reduced to trivial-small magnitudes across graft types at 6 months (BPTB: 0%; HT: 12%).
However, despite the trivial-small asymmetries between legs in knee flexor peak torque at 6 months following reconstruction, graft-related comparisons revealed a large difference in knee flexor LSI with inferior strength recovery in the HT group compared to the BPTB group.
Comparisons across timepoints revealed moderate improvements in knee extensor peak torque in the injured leg, with LSI exceeding 90% for both graft types at 6 months following ACL reconstruction.
The improved knee extensor strength across time was further underpinned by trivial asymmetries between legs at 6 months following surgery for both graft types.Aligning with our results, several previous studies [22, 26-28, 30-32] have reported comparable knee extensor LSI across ACL reconstructions involving either BPTB or HT grafts.
In contrast, some research has demonstrated significantly lower knee extensor LSI with a BPTB graft compared to a HT graft following ACL reconstruction [17,18,20,21].It has been postulated that neural factors such as a higher active motor threshold, reduced motor evoked potentials, brain plasticity, abnormal excitability of both spinal reflexive and corticospinal pathways, and damaged mechanoreceptors may underpin the prolonged weakness in the knee extensors sometimes observed after ACL reconstruction when using a BPTB graft [47].Nevertheless, the bulk of existing research [22, 26-28, 30-32] and the novel findings we provided for a professional athlete sample (i.e., international-level, male soccer players) suggest that both graft types are sufficiently and equally effective in restoring knee extensor strength following ACL reconstruction.However, caution should be taken when following surgery) [21,51], and the slower tendon-to-bone healing process (compared to the bone-to-bone tunnel healing evident in BPTB grafts) [52].Although an almost acceptable knee flexor strength asymmetry between legs of 12% was reached in the HT group in our study, the apparent differences in strength recovery between graft types emphasize that clinicians should ensure that sufficient attention is devoted to hamstring exercises specifically targeting the semitendinosus and gracilis in players receiving a HT graft.
In addition to LSI, the conventional peak torque H:Q has been widely used to screen individuals at risk of sustaining ACL injuries, whereby decreased hamstring strength relative to the quadriceps has been identified as a potential risk factor for ACL injury in athletes [53].
In tion [48].The limb symmetry in knee extensor strength observed in our study indicates that 6 months may be a sufficient recovery timeframe following a suitable rehabilitation programme to restore quadriceps strength in international male soccer players irrespective of using BPTB or HT grafts.In this regard, attaining suitable inter-limb knee extensor symmetry is important among soccer players given that this attribute has been shown to distinguish between different playing levels [14] and negatively correlate with change-of-direction and sprint performance [49], which are key movements performed during competition [50].
Like the knee extensors, we observed moderate-large improvements in knee flexor peak torque in the injured leg across timepoints; however, knee flexor strength reached an equivalent level to the contralateral leg only in the BPTB group, with a strength deficit of 12% apparent in the injured leg for the HT group at 6 months following However, despite some research showing comparable LSI between graft types following reconstruction (19,21,24,26,27), none of these studies demonstrated that the patient samples examined had reached the recommended strength recovery level (LSI > 90%) by 6 months with HT grafts during the rehabilitation process.In turn, the deficit in knee flexor strength with HT grafts compared to BPTB grafts consistently reported across various patient samples following ACL reconstruction may be partly attributed to chronic neuromuscular inhibition of the donor muscle [17], the slow regenerative capacity of the semitendinosus and gracilis tendons (up to 12-24 months

FIG. 1 .
FIG. 1.Mean ± standard deviation for (a) knee extensor peak torque, (b) knee flexor peak torque, (c) peak torque hamstrings:quadriceps ratio, and (d) limb symmetry index (LSI) in international male soccer players who underwent either a bone-patellar tendon-bone (BPTB) graft or hamstring tendon (HT) graft for anterior cruciate ligament reconstruction taken at 3 months and 6 months following surgery during the rehabilitation process.

FIG. 2 .
FIG. 2. Individual data points for each subject and descriptive values for (a) knee extensor peak torque, (b) knee flexor peak torque, (c) peak torque hamstrings:quadriceps ratio, and (d) leg symmetry index in international male soccer players who underwent either a bone-patellar tendon-bone (BPTB) graft or hamstring tendon (HT) graft for anterior cruciate ligament reconstruction taken at 3 months and 6 months following surgery during the rehabilitation process.Note: Each marker represents a different subject.In the box plots, whiskers indicate the minimum and maximum values, the boundary of the box closest to zero indicates the 25 th percentile, the black line within the box indicates the median, and the boundary of the box farthest from zero indicates the 75 th percentile.

FIG. 4 .
FIG. 4.Statistical pairwise comparisons for (a) peak torque hamstrings:quadriceps ratio and (b) leg symmetry index (LSI) between timepoints, legs, muscles, and graft types in international male soccer players.
deficits in assessments due to the greater recruitment of type II muscle fibres[25], which undergo more pronounced atrophy than type I muscle fibres following ACL reconstruc- tion with strength tests to indicate a more complete functional recovery status to support rehabilitative progression and determine readiness to play.Third, although isokinetic strength assessments were performed in a concentric:concentric contraction mode to prevent muscle strains, it should be acknowledged that ACL injuries may